Differential activity of UV-DDB in mouse keratinocytes and fibroblasts: Impact on DNA repair and UV-induced skin cancer

DNA Repair

Volumn 8, Issue 2, 2009, Pages 153-161

  Pines, Alex ^a   Backendorf, Claude ^b   Alekseev, Sergey ^c   Jansen, Jacob G ^a   de Gruijl, Frank R ^a   Vrieling, Harry ^a   Mullenders, Leon H F ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Fibroblast; Keratinocytes; Skin cancer; UV DDB

Indexed keywords

DNA BINDING PROTEIN; DNA BINDING PROTEIN 2; PYRIMIDINE DIMER; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER SUSCEPTIBILITY; CELL FRACTIONATION; DNA BINDING PROTEIN 2 GENE; DNA DAMAGE; DNA REPAIR; EXCISION REPAIR; FIBROBLAST; GENE; GENE EXPRESSION; KERATINOCYTE; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIATION EXPOSURE; RADIATION PROTECTION; SKIN CANCER; SKIN CARCINOGENESIS; SKIN CELL; ULTRAVIOLET B RADIATION; WESTERN BLOTTING; WILD TYPE;

ANIMALS; DISEASE SUSCEPTIBILITY; DNA REPAIR; DNA-BINDING PROTEINS; FIBROBLASTS; HUMANS; KERATINOCYTES; KINETICS; MICE; MICE, HAIRLESS; PYRIMIDINE DIMERS; SKIN NEOPLASMS; ULTRAVIOLET RAYS;

MUS;

EID: 58149144600     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2008.09.011     Document Type: Article

References (52)

1. de Laat W.L., Jaspers N.G., and Hoeijmakers J.H. Molecular mechanism of nucleotide excision repair. Genes Dev. 13 (1999) 768-785
2. Friedberg E.C. How nucleotide excision repair protects against cancer. Nat. Rev. Cancer 1 (2001) 22-33
3. Hwang B.J., Ford J.M., Hanawalt P.C., and Chu G. Expression of the p48 xeroderma pigmentosum gene is p53-dependent and is involved in global genomic repair. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 424-428
4. Itoh T., Mori T., Ohkubo H., and Yamaizumi M. A newly identified patient with clinical xeroderma pigmentosum phenotype has a non-sense mutation in the DDB2 gene and incomplete repair in (6-4) photoproducts. J. Invest. Dermatol. 113 (1999) 251-257
5. Moser J., Volker M., Kool H., Alekseev S., Vrieling H., Yasui A., van Zeeland A.A., and Mullenders L.H. The UV-damaged DNA binding protein mediates efficient targeting of the nucleotide excision repair complex to UV-induced photo lesions. DNA Repair (Amst.) 4 (2005) 571-582
6. Fujiwara Y., Masutani C., Mizukoshi T., Kondo J., Hanaoka F., and Iwai S. Characterization of DNA recognition by the human UV-damaged DNA-binding protein. J. Biol. Chem. 274 (1999) 20027-20033
7. Nichols A.F., Ong P., and Linn S. Mutations specific to the xeroderma pigmentosum group E Ddb- phenotype. J. Biol. Chem. 271 (1996) 24317-24320
8. Rapic-Otrin V., Navazza V., Nardo T., Botta E., McLenigan M., Bisi D.C., Levine A.S., and Stefanini M. True XP group E patients have a defective UV-damaged DNA binding protein complex and mutations in DDB2 which reveal the functional domains of its p48 product. Hum. Mol. Genet. 12 (2003) 1507-1522
9. Hayes S., Shiyanov P., Chen X., and Raychaudhuri P. DDB, a putative DNA repair protein, can function as a transcriptional partner of E2F1. Mol. Cell. Biol. 18 (1998) 240-249
10. Wakasugi M., Kawashima A., Morioka H., Linn S., Sancar A., Mori T., Nikaido O., and Matsunaga T. DDB accumulates at DNA damage sites immediately after UV irradiation and directly stimulates nucleotide excision repair. J. Biol. Chem. 277 (2002) 1637-1640
11. Rapic O., Kuraoka V.I., Nardo T., McLenigan M., Eker A.P., Stefanini M., Levine A.S., and Wood R.D. Relationship of the xeroderma pigmentosum group E DNA repair defect to the chromatin and DNA binding proteins UV-DDB and replication protein A. Mol. Cell. Biol. 18 (1998) 3182-3190
12. Keeney S., Eker A.P., Brody T., Vermeulen W., Bootsma D., Hoeijmakers J.H., and Linn S. Correction of the DNA repair defect in xeroderma pigmentosum group E by injection of a DNA damage-binding protein. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 4053-4056
13. Wang Q.E., Zhu Q., Wani G., Chen J., and Wani A.A. UV radiation-induced XPC translocation within chromatin is mediated by damaged-DNA binding protein, DDB2. Carcinogenesis 25 (2004) 1033-1043
14. Datta A., Bagchi S., Nag A., Shiyanov P., Adami G.R., Yoon T., and Raychaudhuri P. The p48 subunit of the damaged-DNA binding protein DDB associates with the CBP/p300 family of histone acetyltransferase. Mutat. Res. 486 (2001) 89-97
15. Groisman R., Polanowska J., Kuraoka I., Sawada J., Saijo M., Drapkin R., Kisselev A.F., Tanaka K., and Nakatani Y. The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113 (2003) 357-367
16. Sugasawa K., Okuda Y., Saijo M., Nishi R., Matsuda N., Chu G., Mori T., Iwai S., Tanaka K., Tanaka K., and Hanaoka F. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 121 (2005) 387-400
17. Tan T., and Chu G. p53 Binds and activates the xeroderma pigmentosum DDB2 gene in humans but not mice. Mol. Cell. Biol. 22 (2002) 3247-3254
18. Itoh T., Cado D., Kamide R., and Linn S. DDB2 gene disruption leads to skin tumors and resistance to apoptosis after exposure to ultraviolet light but not a chemical carcinogen. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 2052-2057
19. Bohr V.A., Smith C.A., Okumoto D.S., and Hanawalt P.C. DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell 40 (1985) 359-369
20. Vreeswijk M.P., van Hoffen A., Westland B.E., Vrieling H., van Zeeland A.A., and Mullenders L.H. Analysis of repair of cyclobutane pyrimidine dimers and pyrimidine 6-4 pyrimidone photoproducts in transcriptionally active and inactive genes in Chinese hamster cells. J. Biol. Chem. 269 (1994) 31858-31863
21. Cheo D.L., Ruven H.J., Meira L.B., Hammer R.E., Burns D.K., Tappe N.J., van Zeeland A.A., Mullenders L.H., and Friedberg E.C. Characterization of defective nucleotide excision repair in XPC mutant mice. Mutat. Res. 374 (1997) 1-9
22. Klaude M., Gedik C.M., and Collins A.R. DNA damage and repair after low doses of UV-C radiation; comparable rates of repair in rodent and human cells. Int. J. Radiat. Biol. 67 (1995) 501-508
23. Yoon T., Chakrabortty A., Franks R., Valli T., Kiyokawa H., and Raychaudhuri P. Tumor-prone phenotype of the DDB2-deficient mice. Oncogene 24 (2005) 469-478
24. Alekseev S., Kool H., Rebel H., Fousteri M., Moser J., Backendorf C., de Gruijl F.R., Vrieling H., and Mullenders L.H. Enhanced DDB2 expression protects mice from carcinogenic effects of chronic UV-B irradiation. Cancer Res. 65 (2005) 10298-10306
25. Nijhof J.G., van Pelt C., Mulder A.A., Mitchell D.L., Mullenders L.H., de F.R., and Gruijl. Epidermal stem and progenitor cells in murine epidermis accumulate UV damage despite NER proficiency. Carcinogenesis 28 (2007) 792-800
26. Liu W., Nichols A.F., Graham J.A., Dualan R., Abbas A., and Linn S. Nuclear transport of human DDB protein induced by ultraviolet light. J. Biol. Chem. 275 (2000) 21429-21434
27. D'Errico M., Teson M., Calcagnile A., Nardo T., De Luca N., Lazzari C., Soddu S., Zambruno G., Stefanini M., and Dogliotti E. Differential role of transcription-coupled repair in UVB-induced response of human fibroblasts and keratinocytes. Cancer Res. 65 (2005) 432-438
28. Rapic-Otrin V., McLenigan M.P., Bisi D.C., Gonzalez M., and Levine A.S. Sequential binding of UV DNA damage binding factor and degradation of the p48 subunit as early events after UV irradiation. Nucleic Acids Res. 30 (2002) 2588-2598
29. Ishizaki K., Ejima Y., Matsunaga T., Hara R., Sakamoto A., Ikenaga M., Ikawa Y., and Aizawa S. Increased UV-induced SCEs but normal repair of DNA damage in p53-deficient mouse cells. Int. J. Cancer 58 (1994) 254-257
30. Hwang B.J., Toering S., Francke U., and Chu G. p48 Activates a UV-damaged-DNA binding factor and is defective in xeroderma pigmentosum group E cells that lack binding activity. Mol. Cell. Biol. 18 (1998) 4391-4399
31. Rebel H., Mosnier L.O., Berg R.J., Westerman-de Vries A., van Steeg H., van Kranen H.J., and de Gruijl F.R. Early p53-positive foci as indicators of tumor risk in ultraviolet-exposed hairless mice: kinetics of induction, effects of DNA repair deficiency, and p53 heterozygosity. Cancer Res. 61 (2001) 977-983
32. van Zeeland A.A., Smith C.A., and Hanawalt P.C. Sensitive determination of pyrimidine dimers in DNA of UV-irradiated mammalian cells. Introduction of T4 endonuclease V into frozen and thawed cells. Mutat. Res. 82 (1981) 173-189
33. Ivanova I.A., D'Souza S.J., and Dagnino L. E2F1 stability is regulated by a novel-PKC/p38beta MAP kinase signaling pathway during keratinocyte differentiation. Oncogene 25 (2006) 430-437
34. Prost S., Lu P., Caldwell H., and Harrison D. E2F regulates DDB2: consequences for DNA repair in Rb-deficient cells. Oncogene 26 (2007) 3572-3581
35. Ruven H.J., Seelen C.M., Lohman P.H., van Kranen H., van Zeeland A.A., and Mullenders L.H. Strand-specific removal of cyclobutane pyrimidine dimers from the p53 gene in the epidermis of UVB-irradiated hairless mice. Oncogene 9 (1994) 3427-3432
36. Ikehata H., Aiba S., Ozawa H., and Ono T. Thermolysin improves mutation analysis in skin epidermis from ultraviolet light-irradiated Muta Mouse. Environ. Mol. Mutagen. 38 (2001) 55-58
37. Vink A.A., Berg R.J., de Gruijl F.R., Roza L., and Baan R.A. Induction, repair and accumulation of thymine dimers in the skin of UV-B-irradiated hairless mice. Carcinogenesis 12 (1991) 861-864
38. Vink A.A., Henegouwen B., Nikaido O., Baan R.A., and Roza L. Removal of UV-induced DNA lesions in mouse epidermis soon after irradiation. J. Photochem. Photobiol. B 24 (1994) 25-31
39. Berg R.J., Rebel H., van der Horst G.T., van Kranen H.J., Mullenders L.H., van Vloten W.A., and de Gruijl F.R. Impact of global genome repair versus transcription-coupled repair on ultraviolet carcinogenesis in hairless mice. Cancer Res. 60 (2000) 2858-2863
40. Berg R.J., de Vries A., van Steeg H., and de Gruijl F.R. Relative susceptibilities of XPA knockout mice and their heterozygous and wild-type littermates to UVB-induced skin cancer. Cancer Res. 57 (1997) 581-584
41. Itoh T., Iwashita S., Cohen M.B., Meyerholz D.K., and Linn S. Ddb2 is a haploinsufficient tumor suppressor and controls spontaneous germ cell apoptosis. Hum. Mol. Genet. 16 (2007) 1578-1586
42. DiPaolo J.A. Relative difficulties in transforming human and animal cells in vitro. J. Natl. Cancer Inst. 70 (1983) 3-8
43. Sager R., Tanaka K., Lau C.C., Ebina Y., and Anisowicz A. Resistance of human cells to tumorigenesis induced by cloned transforming genes. Proc. Natl. Acad. Sci. U.S.A. 80 (1983) 7601-7605
44. Boukamp P., Petrussevska R.T., Breitkreutz D., Hornung J., Markham A., and Fusenig N.E. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106 (1988) 761-771
45. Backendorf C., de Wit J., van Oosten M., Stout G.J., Mitchell J.R., Borgstein A.M., van der Horst G.T., de Gruijl F.R., Brouwer J., Mullenders L.H., and Hoeijmakers J.H. Repair characteristics and differentiation propensity of long-term cultures of epidermal keratinocytes derived from normal and NER-deficient mice. DNA Repair (Amst.) 4 (2005) 1325-1336
46. Brennan J.K., Mansky J., Roberts G., and Lichtman M.A. Improved methods for reducing calcium and magnesium concentrations in tissue culture medium: application to studies of lymphoblast proliferation in vitro. In Vitro 11 (1975) 354-360
47. Pines A., Perrone L., Bivi N., Romanello M., Damante G., Gulisano M., Kelley M.R., Quadrifoglio F., and Tell G. Activation of APE1/Ref-1 is dependent on reactive oxygen species generated after purinergic receptor stimulation by ATP. Nucleic Acids Res. 33 (2005) 4379-4394
48. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
49. Fousteri M., Vermeulen W., van Zeeland A.A., and Mullenders L.H. Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol. Cell 23 (2006) 471-482
50. Venema J., van Hoffen A., Karcagi V., Natarajan A.T., van Zeeland A.A., and Mullenders L.H. Xeroderma pigmentosum complementation group C cells remove pyrimidine dimers selectively from the transcribed strand of active genes. Mol. Cell. Biol. 11 (1991) 4128-4134
51. Mone M.J., Volker M., Nikaido O., Mullenders L.H., van Zeeland A.A., Verschure P.J., Manders E.M., and van Driel R. Local UV-induced DNA damage in cell nuclei results in local transcription inhibition. EMBO Rep. 2 (2001) 1013-1017
52. Volker M., Mone M.J., Karmakar P., van Hoffen A., Schul W., Vermeulen W., Hoeijmakers J.H., van Driel R., van Zeeland A.A., and Mullenders L.H. Sequential assembly of the nucleotide excision repair factors in vivo. Mol. Cell 8 (2001) 213-224